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Intraoperative in vivo confocal laser endomicroscopy imaging at glioma margins: can we detect tumor infiltration?

Yuan Xu, Andrea M. Mathis, Bianca Pollo, Jürgen Schlegel, Theoni Maragkou, Kathleen Seidel, Philippe Schucht, Kris A. Smith, Randall W. Porter, Andreas Raabe, Andrew S. Little, Nader Sanai, Dennis C. Agbanyim, Nikolay L. Martirosyan, Jennifer M. Eschbacher, Karl Quint, Mark C. Preul, and Ekkehard Hewer

OBJECTIVE

Confocal laser endomicroscopy (CLE) is a US Food and Drug Administration–cleared intraoperative real-time fluorescence-based cellular resolution imaging technology that has been shown to image brain tumor histoarchitecture rapidly in vivo during neuro-oncological surgical procedures. An important goal for successful intraoperative implementation is in vivo use at the margins of infiltrating gliomas. However, CLE use at glioma margins has not been well studied.

METHODS

Matching in vivo CLE images and tissue biopsies acquired at glioma margin regions of interest (ROIs) were collected from 2 institutions. All images were reviewed by 4 neuropathologists experienced in CLE. A scoring system based on the pathological features was implemented to score CLE and H&E images from each ROI on a scale from 0 to 5. Based on the H&E scores, all ROIs were divided into a low tumor probability (LTP) group (scores 0–2) and a high tumor probability (HTP) group (scores 3–5). The concordance between CLE and H&E scores regarding tumor probability was determined. The intraclass correlation coefficient (ICC) and diagnostic performance were calculated.

RESULTS

Fifty-six glioma margin ROIs were included for analysis. Interrater reliability of the scoring system was excellent when used for H&E images (ICC [95% CI] 0.91 [0.86–0.94]) and moderate when used for CLE images (ICC [95% CI] 0.69 [0.40–0.83]). The ICCs (95% CIs) of the LTP group (0.68 [0.40–0.83]) and HTP group (0.68 [0.39–0.83]) did not differ significantly. The concordance between CLE and H&E scores was 61.6%. The sensitivity and specificity values of the scoring system were 79% and 37%. The positive predictive value (PPV) and negative predictive value were 65% and 53%, respectively. Concordance, sensitivity, and PPV were greater in the HTP group than in the LTP group. Specificity was higher in the newly diagnosed group than in the recurrent group.

CONCLUSIONS

CLE may detect tumor infiltration at glioma margins. However, it is not currently dependable, especially in scenarios where low probability of tumor infiltration is expected. The proposed scoring system has excellent intrinsic interrater reliability, but its interrater reliability is only moderate when used with CLE images. These results suggest that this technology requires further exploration as a method for consistent actionable intraoperative guidance with high dependability across the range of tumor margin scenarios. Specific-binding and/or tumor-specific fluorophores, a CLE image atlas, and a consensus guideline for image interpretation may help with the translational utility of CLE.

In Journal of Neurosurgery Publish Before Print

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The biportal transorbital approach: quantitative comparison of the anterior subfrontal craniotomy, bilateral transorbital endoscopic, and microscopic approaches

Lena Mary Houlihan, Thanapong Loymak, Irakliy Abramov, Jubran H. Jubran, Ann J. Staudinger Knoll, Jacob T. Howshar, Michael G. J. O’Sullivan, Michael T. Lawton, and Mark C. Preul

OBJECTIVE

The aim of this study was to assess the surgical use and applicability of a biportal bitransorbital approach. Single-portal transorbital and combined transorbital transnasal approaches have been used in clinical practice, but no study has assessed the surgical use and applicability of a biportal bitransorbital approach.

METHODS

Ten cadaver specimens underwent midline anterior subfrontal (ASub), bilateral transorbital microsurgery (bTMS), and bilateral transorbital neuroendoscopic surgery (bTONES) approaches. Morphometric analyses included the length of the bilateral cranial nerves I and II, the optic tract, and A1; the area of exposure of the anterior cranial fossa floor; craniocaudal and mediolateral angles of attack (AOAs); and volume of surgical freedom (VSF; maximal available working volume for a specific surgical corridor and surgical target structure normalized to a height of 10 mm) of the bilateral paraclinoid internal carotid arteries (ICAs), bilateral terminal ICAs, and anterior communicating artery (ACoA). Analyses were conducted to determine whether the biportal approach was associated with greater instrument freedom.

RESULTS

The bTMS and bTONES approaches provided limited access to the bilateral A1 segments and the ACoA, which were inaccessible in 30% (bTMS) and 60% (bTONES) of exposures. The average total frontal lobe area of exposure (AOE) was 1648.4 mm2 (range 1516.6–1958.8 mm2) for ASub, 1658.9 mm2 (1274.6–1988.2 mm2) for bTMS, and 1914.9 mm2 (1834.2–2014.2 mm2) for bTONES exposures, with no statistically significant superiority between any of the 3 approaches (p = 0.28). The bTMS and bTONES approaches were significantly associated with decreases of 8.7 mm3 normalized volume (p = 0.005) and 14.3 mm3 normalized volume (p < 0.001) for VSF of the right paraclinoid ICA compared with the ASub approach. No statistically significant difference in surgical freedom was noted between all 3 approaches when targeting the bilateral terminal ICA. The bTONES approach was significantly associated with a decrease of 105% in the (log) VSF of the ACoA compared with the ASub (p = 0.009).

CONCLUSIONS

Although the biportal approach is intended to improve maneuverability within these minimally invasive approaches, these results illustrate the pertinent issue of surgical corridor crowding and the importance of surgical trajectory planning. A biportal transorbital approach provides improved visualization but does not improve surgical freedom. Furthermore, although it affords impressive anterior cranial fossa AOE, it is unsuitable for addressing midline lesions because the preserved orbital rim restricts lateral movement. Further comparative studies will elucidate whether a combined transorbital transnasal route is preferable to minimize skull base destruction and maximize instrument access.

In Journal of Neurosurgery Publish Before Print

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Quantification of motion during microvascular anastomosis simulation using machine learning hand detection

Nicolas I. Gonzalez-Romo, Sahin Hanalioglu, Giancarlo Mignucci-Jiménez, Grant Koskay, Irakliy Abramov, Yuan Xu, Wonhyoung Park, Michael T. Lawton, and Mark C. Preul

OBJECTIVE

Microanastomosis is one of the most technically demanding and important microsurgical skills for a neurosurgeon. A hand motion detector based on machine learning tracking technology was developed and implemented for performance assessment during microvascular anastomosis simulation.

METHODS

A microanastomosis motion detector was developed using a machine learning model capable of tracking 21 hand landmarks without physical sensors attached to a surgeon’s hands. Anastomosis procedures were simulated using synthetic vessels, and hand motion was recorded with a microscope and external camera. Time series analysis was performed to quantify the economy, amplitude, and flow of motion using data science algorithms. Six operators with various levels of technical expertise (2 experts, 2 intermediates, and 2 novices) were compared.

RESULTS

The detector recorded a mean (SD) of 27.6 (1.8) measurements per landmark per second with a 10% mean loss of tracking for both hands. During 600 seconds of simulation, the 4 nonexperts performed 26 bites in total, with a combined excess of motion of 14.3 (15.5) seconds per bite, whereas the 2 experts performed 33 bites (18 and 15 bites) with a mean (SD) combined excess of motion of 2.8 (2.3) seconds per bite for the dominant hand. In 180 seconds, the experts performed 13 bites, with mean (SD) latencies of 22.2 (4.4) and 23.4 (10.1) seconds, whereas the 2 intermediate operators performed a total of 9 bites with mean (SD) latencies of 31.5 (7.1) and 34.4 (22.1) seconds per bite.

CONCLUSIONS

A hand motion detector based on machine learning technology allows the identification of gross and fine movements performed during microanastomosis. Economy, amplitude, and flow of motion were measured using time series data analysis. Technical expertise could be inferred from such quantitative performance analysis.

In Neurosurgical Focus Volume 54 (2023): Issue 6 (Jun 2023): Machine Learning in Neurosurgery

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Erratum. Artery of Uchimura: origin and evolution of identification of the vascular supply to the hippocampus

Mark C. Preul

In Journal of Neurosurgery Publish Before Print

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Artery of Uchimura: origin and evolution of identification of the vascular supply to the hippocampus

Ali Tayebi Meybodi, Giancarlo Mignucci-Jiménez, Yuan Xu, and Mark C. Preul

In 1928, neuroscientist Yushi Uchimura (1897–1980) published a landmark study detailing the hippocampal vasculature. Working in Walther Spielmeyer’s Munich laboratory (1925–1927), Uchimura sought evidence for a vascular theory of Ammon’s horn sclerosis (AHS). He described an artery supplying the vulnerable sector of the hippocampus, where pathognomonic changes of AHS were noted, and characterized the artery as particularly susceptible to circulatory disturbances. Discovery of this artery led to new concepts and new terminology pertaining to the hippocampus. In addition to having a distinguished career in psychiatry and academia (including a position as University of Tokyo dean), Uchimura was, before attending medical school, one of Japan’s best baseball pitchers; he was eventually named Nippon Professional Baseball Organization commissioner and inducted into the Japan Baseball Hall of Fame. Uchimura’s description of hippocampal vasculature, which is still subject to debate after nearly a century, brought international attention to AHS and epilepsy and showed the hippocampal vasculature to be variable and vulnerable; important considerations for later neurosurgeons in the development of selective mesial temporal surgery. Prominent figures in neurosurgery have since developed classification systems for the hippocampal vasculature in which the artery of Uchimura remains central. Perhaps no other brain artery has been the nexus for such intense investigation and debate about its association to structure, function, disease, and treatment methodology.

In Journal of Neurosurgery Publish Before Print

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Combined subtarsal contralateral transmaxillary retroeustachian and endoscopic endonasal approaches to the infrapetrous region

Mohamed A. Labib, Irakliy Abramov, Lena Mary Houlihan, Visish M. Srinivasan, Lea Scherschinski, Daniel M. Prevedello, Ricardo L. Carrau, Hussam Abou-Al-Shaar, Mark C. Preul, and Michael T. Lawton

OBJECTIVE

The eustachian tube (ET) limits endoscopic endonasal access to the infrapetrous region. Transecting or mobilizing the ET may result in morbidities. This study presents a novel approach in which a subtarsal contralateral transmaxillary (ST-CTM) corridor is coupled with the standard endonasal approach to facilitate access behind the intact ET.

METHODS

Eight cadaveric head specimens were dissected. Endoscopic endonasal approaches (EEAs) (i.e., transpterygoid and inferior transclival) were performed on one side, followed by ST-CTM and sublabial contralateral transmaxillary (SL-CTM) approaches on the opposite side, along with different ET mobilization techniques on the original side. Seven comparative groups were generated. The length of the cranial nerves, areas of exposure, and volume of surgical freedom (VSF) in the infrapetrous regions were measured and compared.

RESULTS

Without ET mobilization, the combined ST-CTM/EEA approach provided greater exposure than EEA alone (mean ± SD 288.9 ± 40.66 mm2 vs 91.7 ± 49.9 mm2; p = 0.001). The VSFs at the ventral jugular foramen (JF), entrance to the petrous internal carotid artery (ICA), and lateral to the parapharyngeal ICA were also greater in ST-CTM/EEA than in EEA alone (p = 0.002, p = 0.002, and p < 0.001, respectively). EEA alone, however, provided greater VSF at the hypoglossal canal (HGC) than did ST-CTM/EEA (p = 0.01). The SL-CTM approach did not increase the EEA exposure (p = 0.48). The ST-CTM/EEA approach provided greater exposure than EEA with extended inferolateral (EIL) or anterolateral (AL) ET mobilization (p = 0.001 and p = 0.02, respectively). The ST-CTM/EEA also increased the VSF lateral to the parapharyngeal ICA in comparison with EEA/EIL ET mobilization (p < 0.001) but not with EEA/AL ET mobilization (p = 0.36). Finally, the VSFs at the HGC and JF were greater in EEA/AL ET mobilization than in ST-CTM/EEA without ET mobilization (p = 0.002 and p = 0.004, respectively).

CONCLUSIONS

Combining the EEA with the more laterally and superiorly originating ST-CTM approach allows greater exposure of the infrapetrous and ventral JF regions while obviating the need for mobilizing the ET. The surgical freedom afforded by the combined approaches is greater than that obtained by EEA alone.

In Journal of Neurosurgery Publish Before Print

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Introduction. On forging a new specialty from the crucible of war

Charles J. Prestigiacomo, Mark C. Preul, T. Forcht Dagi, Chris J. Neal, Jeffrey V. Rosenfeld, and Melissa Meister

In Neurosurgical Focus Volume 53 (2022): Issue 3 (Sep 2022): World History of Military Neurosurgery

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Management of injuries on the 16th-century battlefield: Ambroise Paré’s contributions to neurosurgery and functional recovery

Marian T. Park, Giancarlo Mignucci-Jiménez, Lena Mary Houlihan, and Mark C. Preul

During the 1536 siege of Turin in northern Italy, a young French barber-surgeon abandoned the conventional treatment of battle-inflicted wounds, launching a revolution in military medicine and surgical techniques. Ambroise Paré (1510–1590) was born into a working-class Huguenot family in Laval, France, during an era when surgery was not considered a respectable profession. He rose from humble origins as a barber-surgeon, a low-ranked occupation in the French medical hierarchy, to become a royal surgeon (chirurgien ordinaire du Roi) serving 4 consecutive French monarchs. His innovative ideas and surgical practice were a response to the environment created by new military technology on 16th-century European battlefields. Gunpowder weapons caused unfamiliar, complicated injuries that challenged Paré to develop new techniques and surgical instruments. Although Paré’s contributions to the treatment of wounds and functional prosthetics are documented, a deeper appreciation of his role in military neurosurgery is needed. This paper examines archives, primary texts, and written accounts by Paré that reveal specific patient cases highlighting his innovative contributions to neurotrauma and neurosurgery during demanding and harrowing circumstances, on and off the battlefield, in 16th-century France. Notably, trepanation indications increased because of battlefield head injuries, and Paré frequently described this technique and improved the design of the trepan tool. His contribution to neurologically related topics is extensive; there are more chapters devoted to the nervous system than to any other organ system in his compendium, Oeuvres. Regarding anatomical knowledge as fundamentally important and admiring the contemporary contributions of Andreas Vesalius, Paré reproduced many images from Vesalius’ works at his own great expense. The manner in which Paré’s participation in military expeditions enabled collaboration with multidisciplinary artisans on devices, including surgical tools and prosthetics, to restore neurologically associated functionality is also discussed. Deeply religious, in a life filled with adventure, and serving in often horrendous conditions during a time when Galenic dogma still dominated medical practice, Paré developed a reputation for logic, empiricism, technology, and careful treatment. "I have [had] the opportunity to praise God, for what he called me to do in medical operation, which is commonly called surgery, which could not be bought with gold or silver, but by only virtue and great experimentation."

In Neurosurgical Focus Volume 53 (2022): Issue 3 (Sep 2022): World History of Military Neurosurgery

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Seven bypasses simulation set: description and validity assessment of novel models for microneurosurgical training

Evgenii Belykh, Irakliy Abramov, Liudmila Bardonova, Ruchi Patel, Sarah McBryan, Lara Enriquez Bouza, Neil Majmundar, Xiaochun Zhao, Vadim A. Byvaltsev, Stephen A. Johnson, Amit Singla, Gaurav Gupta, Hai Sun, James K. Liu, Anil Nanda, Mark C. Preul, and Michael T. Lawton

OBJECTIVE

Microsurgical training remains indispensable to master cerebrovascular bypass procedures, but simulation models for training that accurately replicate microanastomosis in narrow, deep-operating corridors are lacking. Seven simulation bypass scenarios were developed that included head models in various surgical positions with premade approaches, simulating the restrictions of the surgical corridors and hand positions for microvascular bypass training. This study describes these models and assesses their validity.

METHODS

Simulation models were created using 3D printing of the skull with a designed craniotomy. Brain and external soft tissues were cast using a silicone molding technique from the clay-sculptured prototypes. The 7 simulation scenarios included: 1) temporal craniotomy for a superficial temporal artery (STA)–middle cerebral artery (MCA) bypass using the M4 branch of the MCA; 2) pterional craniotomy and transsylvian approach for STA-M2 bypass; 3) bifrontal craniotomy and interhemispheric approach for side-to-side bypass using the A3 branches of the anterior cerebral artery; 4) far lateral craniotomy and transcerebellomedullary approach for a posterior inferior cerebellar artery (PICA)–PICA bypass or 5) PICA reanastomosis; 6) orbitozygomatic craniotomy and transsylvian-subtemporal approach for a posterior cerebral artery bypass; and 7) extended retrosigmoid craniotomy and transcerebellopontine approach for an occipital artery–anterior inferior cerebellar artery bypass. Experienced neurosurgeons evaluated each model by practicing the aforementioned bypasses on the models. Face and content validities were assessed using the bypass participant survey.

RESULTS

A workflow for model production was developed, and these models were used during microsurgical courses at 2 neurosurgical institutions. Each model is accompanied by a corresponding prototypical case and surgical video, creating a simulation scenario. Seven experienced cerebrovascular neurosurgeons practiced microvascular anastomoses on each of the models and completed surveys. They reported that actual anastomosis within a specific approach was well replicated by the models, and difficulty was comparable to that for real surgery, which confirms the face validity of the models. All experts stated that practice using these models may improve bypass technique, instrument handling, and surgical technique when applied to patients, confirming the content validity of the models.

CONCLUSIONS

The 7 bypasses simulation set includes novel models that effectively simulate surgical scenarios of a bypass within distinct deep anatomical corridors, as well as hand and operator positions. These models use artificial materials, are reusable, and can be implemented for personal training and during microsurgical courses.

In Journal of Neurosurgery Volume 138: Issue 3 (Mar 2023)

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Intraoperative confocal laser endomicroscopy: prospective in vivo feasibility study of a clinical-grade system for brain tumors

Irakliy Abramov, Marian T. Park, Evgenii Belykh, Alexander B. Dru, Yuan Xu, Timothy C. Gooldy, Lea Scherschinski, S. Harrison Farber, Andrew S. Little, Randall W. Porter, Kris A. Smith, Michael T. Lawton, Jennifer M. Eschbacher, and Mark C. Preul

OBJECTIVE

The authors evaluated the feasibility of using the first clinical-grade confocal laser endomicroscopy (CLE) system using fluorescein sodium for intraoperative in vivo imaging of brain tumors.

METHODS

A CLE system cleared by the FDA was used in 30 prospectively enrolled patients with 31 brain tumors (13 gliomas, 5 meningiomas, 6 other primary tumors, 3 metastases, and 4 reactive brain tissue). A neuropathologist classified CLE images as interpretable or noninterpretable. Images were compared with corresponding frozen and permanent histology sections, with image correlation to biopsy location using neuronavigation. The specificities and sensitivities of CLE images and frozen sections were calculated using permanent histological sections as the standard for comparison. A recently developed surgical telepathology software platform was used in 11 cases to provide real-time intraoperative consultation with a neuropathologist.

RESULTS

Overall, 10,713 CLE images from 335 regions of interest were acquired. The mean duration of the use of the CLE system was 7 minutes (range 3–18 minutes). Interpretable CLE images were obtained in all cases. The first interpretable image was acquired within a mean of 6 (SD 10) images and within the first 5 (SD 13) seconds of imaging; 4896 images (46%) were interpretable. Interpretable image acquisition was positively correlated with study progression, number of cases per surgeon, cumulative length of CLE time, and CLE time per case (p ≤ 0.01). The diagnostic accuracy, sensitivity, and specificity of CLE compared with frozen sections were 94%, 94%, and 100%, respectively, and the diagnostic accuracy, sensitivity, and specificity of CLE compared with permanent histological sections were 92%, 90%, and 94%, respectively. No difference was observed between lesion types for the time to first interpretable image (p = 0.35). Deeply located lesions were associated with a higher percentage of interpretable images than superficial lesions (p = 0.02). The study met the primary end points, confirming the safety and feasibility and acquisition of noninvasive digital biopsies in all cases. The study met the secondary end points for the duration of CLE use necessary to obtain interpretable images. A neuropathologist could interpret the CLE images in 29 (97%) of 30 cases.

CONCLUSIONS

The clinical-grade CLE system allows in vivo, intraoperative, high-resolution cellular visualization of tissue microstructure and identification of lesional tissue patterns in real time, without the need for tissue preparation.

In Journal of Neurosurgery Volume 138: Issue 3 (Mar 2023)